Cartography of teneurin and latrophilin expression reveals spatiotemporal axis heterogeneity in the mouse hippocampus during development
Cartography of teneurin and latrophilin expression reveals spatiotemporal axis heterogeneity in the mouse hippocampus during development
Synaptic adhesion molecules (SAMs) are evolutionarily conserved proteins that play an important role in the form and function of neuronal synapses. Teneurins (Tenms) and latrophilins (Lphns) are well-known cell adhesion molecules that form a transsynaptic complex. Recent studies suggest that Tenm3 and Lphn2 (gene symbol Adgrl2) are involved in hippocampal circuit assembly via their topographical expression. However, it is not known whether other teneurins and latrophilins display similar topographically restricted expression patterns during embryonic and postnatal development. Here, we reveal the cartography of all teneurin (Tenm1-4) and latrophilin (Lphn1-3 [Adgrl1-3]) paralog expression in the mouse hippocampus across prenatal and postnatal development as monitored by large-scale single-molecule RNA in situ hybridization mapping. Our results identify a striking heterogeneity in teneurin and latrophilin expression along the spatiotemporal axis of the hippocampus. Tenm2 and Tenm4 expression levels peak at the neonatal stage when compared to Tenm1 and Tenm3, while Tenm1 expression is restricted to the postnatal pyramidal cell layer. Tenm4 expression in the dentate gyrus (DG) exhibits an opposing topographical expression pattern in the embryonic and neonatal hippocampus. Our findings were validated by analyses of multiple RNA-seq datasets at bulk, single-cell, and spatial levels. Thus, our study presents a comprehensive spatiotemporal map of Tenm and Lphn expression in the hippocampus, showcasing their diverse expression patterns across developmental stages in distinct spatial axes.
Animals, Female, Gene Expression Regulation, Developmental, Hippocampus/metabolism, Male, Mice, Mice, Inbred C57BL, Nerve Tissue Proteins/metabolism, Receptors, G-Protein-Coupled, Receptors, Peptide/metabolism, Tenascin
Liakath-Ali, Kif
8d5a020c-e976-4901-9195-68f4bc0de74e
Refaee, Rebecca
3e05b547-3f71-43ef-a73c-99a3dacf23ce
Südhof, Thomas C.
172ec4da-ad42-4b1f-bd99-6b7d288e040c
7 May 2024
Liakath-Ali, Kif
8d5a020c-e976-4901-9195-68f4bc0de74e
Refaee, Rebecca
3e05b547-3f71-43ef-a73c-99a3dacf23ce
Südhof, Thomas C.
172ec4da-ad42-4b1f-bd99-6b7d288e040c
Liakath-Ali, Kif, Refaee, Rebecca and Südhof, Thomas C.
(2024)
Cartography of teneurin and latrophilin expression reveals spatiotemporal axis heterogeneity in the mouse hippocampus during development.
PLoS Biology, 22 (5), [e3002599].
(doi:10.1371/journal.pbio.3002599).
Abstract
Synaptic adhesion molecules (SAMs) are evolutionarily conserved proteins that play an important role in the form and function of neuronal synapses. Teneurins (Tenms) and latrophilins (Lphns) are well-known cell adhesion molecules that form a transsynaptic complex. Recent studies suggest that Tenm3 and Lphn2 (gene symbol Adgrl2) are involved in hippocampal circuit assembly via their topographical expression. However, it is not known whether other teneurins and latrophilins display similar topographically restricted expression patterns during embryonic and postnatal development. Here, we reveal the cartography of all teneurin (Tenm1-4) and latrophilin (Lphn1-3 [Adgrl1-3]) paralog expression in the mouse hippocampus across prenatal and postnatal development as monitored by large-scale single-molecule RNA in situ hybridization mapping. Our results identify a striking heterogeneity in teneurin and latrophilin expression along the spatiotemporal axis of the hippocampus. Tenm2 and Tenm4 expression levels peak at the neonatal stage when compared to Tenm1 and Tenm3, while Tenm1 expression is restricted to the postnatal pyramidal cell layer. Tenm4 expression in the dentate gyrus (DG) exhibits an opposing topographical expression pattern in the embryonic and neonatal hippocampus. Our findings were validated by analyses of multiple RNA-seq datasets at bulk, single-cell, and spatial levels. Thus, our study presents a comprehensive spatiotemporal map of Tenm and Lphn expression in the hippocampus, showcasing their diverse expression patterns across developmental stages in distinct spatial axes.
Text
journal.pbio.3002599
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Accepted/In Press date: 26 March 2024
Published date: 7 May 2024
Keywords:
Animals, Female, Gene Expression Regulation, Developmental, Hippocampus/metabolism, Male, Mice, Mice, Inbred C57BL, Nerve Tissue Proteins/metabolism, Receptors, G-Protein-Coupled, Receptors, Peptide/metabolism, Tenascin
Identifiers
Local EPrints ID: 491384
URI: http://eprints.soton.ac.uk/id/eprint/491384
ISSN: 1544-9173
PURE UUID: a12f514c-c47d-4ac6-be41-ad23cf8d4db0
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Date deposited: 21 Jun 2024 16:34
Last modified: 22 Jun 2024 02:14
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Author:
Kif Liakath-Ali
Author:
Rebecca Refaee
Author:
Thomas C. Südhof
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